Osteonecrosis as a manifestation of Long-COVID Syndrome: a systematic review.
SARS-CoV-2; COVID-19; Osteonecrosis; Systematic review
Journal
Musculoskeletal surgery
ISSN: 2035-5114
Titre abrégé: Musculoskelet Surg
Pays: Italy
ID NLM: 101498346
Informations de publication
Date de publication:
01 Aug 2024
01 Aug 2024
Historique:
received:
08
04
2024
accepted:
25
07
2024
medline:
1
8
2024
pubmed:
1
8
2024
entrez:
31
7
2024
Statut:
aheadofprint
Résumé
Purpose SARS-CoV-2 is an RNA virus responsible for COVID-19 pandemic. Some authors described the set of persistent symptoms COVID-related as "Long-COVID Syndrome." Several cases of post-COVID-19 osteonecrosis (ON) are described. Our primary aim was to study the hypothetical correlation between SARS-CoV-2 infection and ON; our secondary aim was to understand if ON can be considered part of Long-COVID. Materials and methods We performed a systematic review following the Preferred Reporting Items for Systematic Reviewers and Meta-analysis (PRISMA) guidelines. Because COVID-19 is a recently described disease, we included all levels of evidence studies. We excluded studies lacking specification regarding the use of corticosteroids (CCS) and studies not related to COVID-19. The variables extracted were age, sex, risk factors, affected joints, signs and symptoms, magnetic resonance imaging (MRI) and X-ray features, histology, treatment of COVID-19, dose and duration of treatment with CCS, treatment of ON, follow-up, and treatment outcome. Results A total of 13 studies were included, involving 95 patients and 159 joints. Time between the diagnosis of COVID-19 and the onset of symptoms related to ON was 16 weeks on average. Time between the onset of symptoms and the MRI was 6 weeks. An average of 926.4 mg of prednisolone equivalent per patient were administered. On average, CCS were administered for 20.6 days. Conclusions Patients with a history of COVID-19 infection developed osteonecrosis prematurely and with a lower dose of CCS than usually reported in the literature. Symptoms of osteonecrosis occur within the interval of the period described as Long-COVID. Surgeons should not underestimate the persistence of arthralgia when a history of SARS-CoV-2 infection and use of CCS is reported.
Identifiants
pubmed: 39085687
doi: 10.1007/s12306-024-00854-w
pii: 10.1007/s12306-024-00854-w
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Istituto Ortopedico Rizzoli.
Références
Faldini C, Mazzotti A, Arceri A et al (2022) Covid-19 orthopedic trauma patients characteristics and management during the first pandemic period: report from a single institution in Italy. Musculoskelet Surg 106:407–426. https://doi.org/10.1007/s12306-021-00715-w
doi: 10.1007/s12306-021-00715-w
pubmed: 34075546
Compagnoni R, Cucchi D, Klumpp R et al (2023) Operational strategies to deal with the COVID-19 emergency: recommendations from the Italian national society SIAGASCOT following the introduction of vaccines against the SARS-CoV-2 infection. Musculoskelet Surg 107:471–479. https://doi.org/10.1007/s12306-023-00796-9
doi: 10.1007/s12306-023-00796-9
pubmed: 37658981
pmcid: 10709259
Papalia GF, Petrucci G, Russo F et al (2022) COVID-19 pandemic increases the impact of low back pain: a systematic review and metanalysis. Int J Environ Res Public Health 19:4599. https://doi.org/10.3390/ijerph19084599
doi: 10.3390/ijerph19084599
pubmed: 35457462
pmcid: 9027663
Rubin R (2020) As their numbers grow, COVID-19 “long haulers” stump experts. JAMA 324:1381. https://doi.org/10.1001/jama.2020.17709
doi: 10.1001/jama.2020.17709
pubmed: 32965460
Lopez-Leon S, Wegman-Ostrosky T, Perelman C et al (2021) More than 50 long-term effects of COVID-19: a systematic review and meta-analysis. Sci Rep 11:16144. https://doi.org/10.1038/s41598-021-95565-8
doi: 10.1038/s41598-021-95565-8
pubmed: 34373540
pmcid: 8352980
Michelen M, Manoharan L, Elkheir N et al (2021) Characterising long COVID: a living systematic review. BMJ Glob Health 6:e005427. https://doi.org/10.1136/bmjgh-2021-005427
doi: 10.1136/bmjgh-2021-005427
pubmed: 34580069
Pires RE, Reis IGN, Waldolato GS et al (2022) What do we need to know about musculoskeletal manifestations of COVID-19?: A systematic review. JBJS Rev. https://doi.org/10.2106/JBJS.RVW.22.00013
doi: 10.2106/JBJS.RVW.22.00013
pubmed: 35658089
Kantor H (1987) Bone marrow pressure in osteonecrosis of the femoral condyle (Ahlbäck’s disease). Arch Orthop Trauma Surg 106:349–352. https://doi.org/10.1007/BF00456868
doi: 10.1007/BF00456868
pubmed: 3435234
Arnoldi CC, Lemperg K, Linderholm H (1975) Intraosseous hypertension and pain in the knee. J Bone Joint Surg Br 57:360–363
doi: 10.1302/0301-620X.57B3.360
pubmed: 1158947
Baig AM (2021) Chronic COVID syndrome: need for an appropriate medical terminology for long-COVID and COVID long-haulers. J Med Virol 93:2555–2556. https://doi.org/10.1002/jmv.26624
doi: 10.1002/jmv.26624
pubmed: 33095459
Marshall M (2020) The lasting misery of coronavirus long-haulers. Nature 585:339–341. https://doi.org/10.1038/d41586-020-02598-6
doi: 10.1038/d41586-020-02598-6
pubmed: 32929257
Akbarialiabad H, Taghrir MH, Abdollahi A et al (2021) Long COVID, a comprehensive systematic scoping review. Infection 49:1163–1186. https://doi.org/10.1007/s15010-021-01666-x
doi: 10.1007/s15010-021-01666-x
pubmed: 34319569
pmcid: 8317481
Cabrera Martimbianco AL, Pacheco RL, Bagattini ÂM, Riera R (2021) Frequency, signs and symptoms, and criteria adopted for long COVID-19: a systematic review. Int J Clin Pract. https://doi.org/10.1111/ijcp.14357
doi: 10.1111/ijcp.14357
pubmed: 33977626
Excellence N (2020) COVID-19 rapid guideline: managing the long-term effects of COVID-19. National Institute for Health and Care Excellence, London
Greenhalgh T, Knight M, A’Court C et al (2020) Management of post-acute covid-19 in primary care. BMJ. https://doi.org/10.1136/bmj.m3026
doi: 10.1136/bmj.m3026
pubmed: 33106283
Sudre CH, Murray B, Varsavsky T et al (2021) Attributes and predictors of long COVID. Nat Med 27:626–631. https://doi.org/10.1038/s41591-021-01292-y
doi: 10.1038/s41591-021-01292-y
pubmed: 33692530
pmcid: 7611399
Tenforde MW, Kim SS, Lindsell CJ et al (2020) Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network—United States, 2020. MMWR Morb Mortal Wkly Rep 69:993–998. https://doi.org/10.15585/mmwr.mm6930e1
doi: 10.15585/mmwr.mm6930e1
pubmed: 32730238
pmcid: 7392393
Townsend L, Dowds J, O’Brien K et al (2021) Persistent poor health after COVID-19 is not associated with respiratory complications or initial disease severity. Ann Am Thorac Soc 18:997–1003. https://doi.org/10.1513/AnnalsATS.202009-1175OC
doi: 10.1513/AnnalsATS.202009-1175OC
pubmed: 33413026
pmcid: 8456724
Shah W, Hillman T, Playford ED, Hishmeh L (2021) Managing the long term effects of covid-19: summary of NICE, SIGN, and RCGP rapid guideline. BMJ. https://doi.org/10.1136/bmj.n136
doi: 10.1136/bmj.n136
pubmed: 34789505
pmcid: 8548918
Disser NP, De Micheli AJ, Schonk MM et al (2020) Musculoskeletal consequences of COVID-19. J Bone Jt Surg 102:1197–1204. https://doi.org/10.2106/JBJS.20.00847
doi: 10.2106/JBJS.20.00847
Hasan LK, Deadwiler B, Haratian A et al (2021) Effects of COVID-19 on the musculoskeletal system: clinician’s guide. Orthop Res Rev 13:141–150. https://doi.org/10.2147/ORR.S321884
doi: 10.2147/ORR.S321884
pubmed: 34584465
pmcid: 8464590
Widyadharma IPE, Sari NNSP, Pradnyaswari KE et al (2020) Pain as clinical manifestations of COVID-19 infection and its management in the pandemic era: a literature review. Egypt J Neurol Psychiatry Neurosurg 56:121. https://doi.org/10.1186/s41983-020-00258-0
doi: 10.1186/s41983-020-00258-0
Garg M, Maralakunte M, Garg S et al (2021) The conundrum of ‘Long-COVID-19’: a narrative review. Int J Gen Med 14:2491–2506. https://doi.org/10.2147/IJGM.S316708
doi: 10.2147/IJGM.S316708
pubmed: 34163217
pmcid: 8214209
Hoong CWS, Amin MNME, Tan TC, Lee JE (2021) Viral arthralgia a new manifestation of COVID-19 infection? A cohort study of COVID-19-associated musculoskeletal symptoms. Int J Infect Dis 104:363–369. https://doi.org/10.1016/j.ijid.2021.01.031
doi: 10.1016/j.ijid.2021.01.031
pubmed: 33476761
pmcid: 7813485
Karaarslan F, Demircioğlu Güneri F, Kardeş S (2021) Postdischarge rheumatic and musculoskeletal symptoms following hospitalization for COVID-19: prospective follow-up by phone interviews. Rheumatol Int 41:1263–1271. https://doi.org/10.1007/s00296-021-04882-8
doi: 10.1007/s00296-021-04882-8
pubmed: 33978818
pmcid: 8114015
Mahmoud MH, Alghamdi FA, Alghamdi GA et al (2021) Study of post-COVID-19 syndrome in Saudi Arabia. Cureus. https://doi.org/10.7759/cureus.17787
doi: 10.7759/cureus.17787
pubmed: 35141098
pmcid: 8802020
Anaya J-M, Rojas M, Salinas ML et al (2021) Post-COVID syndrome. A case series and comprehensive review. Autoimmun Rev 20:102947. https://doi.org/10.1016/j.autrev.2021.102947
doi: 10.1016/j.autrev.2021.102947
pubmed: 34509649
pmcid: 8428988
Qin ES, Gold LS, Hough CL et al (2022) PATIENT-REPORTED functional outcomes 30 days after hospitalization for COVID-19. PM&R 14:173–182. https://doi.org/10.1002/pmrj.12716
doi: 10.1002/pmrj.12716
Zhang B, Zhang S (2020) Corticosteroid-Induced Osteonecrosis in COVID-19: a call for caution. J Bone Miner Res Off J Am Soc Bone Miner Res 35:1828–1829. https://doi.org/10.1002/jbmr.4136
doi: 10.1002/jbmr.4136
Jafarnezhadgero AA, Hamlabadi MP, Sajedi H, Granacher U (2022) Recreational runners who recovered from COVID-19 show different running kinetics and muscle activities compared with healthy controls. Gait Posture 91:260–265. https://doi.org/10.1016/j.gaitpost.2021.11.002
doi: 10.1016/j.gaitpost.2021.11.002
pubmed: 34775229
Vannini F, Mazzotti A, Stefanini N, Faldini C (2020) Coronavirus disease 2019 pandemic: should we delay cartilage regenerative procedures and accept the consequences, or can we find a new normality? Int Orthop 44:2189–2190. https://doi.org/10.1007/s00264-020-04741-4
doi: 10.1007/s00264-020-04741-4
pubmed: 32767087
Zhao R, Wang H, Wang X, Feng F (2017) Steroid therapy and the risk of osteonecrosis in SARS patients: a dose-response meta-analysis. Osteoporos Int 28:1027–1034. https://doi.org/10.1007/s00198-016-3824-z
doi: 10.1007/s00198-016-3824-z
pubmed: 27844132
Zhang N-F, Li ZR, Wei H-Y et al (2008) Steroid-induced osteonecrosis: the number of lesions is related to the dosage. J Bone Joint Surg Br 90-B:1239–1243. https://doi.org/10.1302/0301-620X.90B9.20056
doi: 10.1302/0301-620X.90B9.20056
Higgins V, Sohaei D, Diamandis EP, Prassas I (2021) COVID-19: from an acute to chronic disease? Potential long-term health consequences. Crit Rev Clin Lab Sci 58:297–310. https://doi.org/10.1080/10408363.2020.1860895
doi: 10.1080/10408363.2020.1860895
pubmed: 33347790
Giannis D, Ziogas IA, Gianni P (2020) Coagulation disorders in coronavirus infected patients: COVID-19, SARS-CoV-1, MERS-CoV and lessons from the past. J Clin Virol 127:104362. https://doi.org/10.1016/j.jcv.2020.104362
doi: 10.1016/j.jcv.2020.104362
pubmed: 32305883
pmcid: 7195278
Liu P, Lee S, Knoll J et al (2017) Loss of menin in osteoblast lineage affects osteocyte–osteoclast crosstalk causing osteoporosis. Cell Death Differ 24:672–682. https://doi.org/10.1038/cdd.2016.165
doi: 10.1038/cdd.2016.165
pubmed: 28106886
pmcid: 5384024
Kotake S, Udagawa N, Takahashi N et al (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103:1345–1352. https://doi.org/10.1172/JCI5703
doi: 10.1172/JCI5703
pubmed: 10225978
pmcid: 408356
Gilbert L, He X, Farmer P et al (2000) Inhibition of osteoblast differentiation by tumor necrosis factor–α*. Endocrinology 141:3956–3964. https://doi.org/10.1210/endo.141.11.7739
doi: 10.1210/endo.141.11.7739
pubmed: 11089525
Awosanya OD, Dalloul CE, Blosser RJ et al (2022) Osteoclast-mediated bone loss observed in a COVID-19 mouse model. Bone 154:116227. https://doi.org/10.1016/j.bone.2021.116227
doi: 10.1016/j.bone.2021.116227
pubmed: 34607050
Haudenschild AK, Christiansen BA, Orr S et al (2023) Acute bone loss following SARS-CoV-2 infection in mice. J Orthop Res. https://doi.org/10.1002/jor.25537
doi: 10.1002/jor.25537
pubmed: 36815216
Gao J, Mei H, Sun J et al (2022) Neuropilin-1-mediated SARS-CoV-2 infection in bone marrow-derived macrophages inhibits osteoclast differentiation. Adv Biol 6:2200007. https://doi.org/10.1002/adbi.202200007
doi: 10.1002/adbi.202200007
Prieto-Pérez L, Fortes J, Soto C et al (2020) Histiocytic hyperplasia with hemophagocytosis and acute alveolar damage in COVID-19 infection. Mod Pathol 33:2139–2146. https://doi.org/10.1038/s41379-020-0613-1
doi: 10.1038/s41379-020-0613-1
pubmed: 32620916
pmcid: 7333227
Wang X, Wen Y, Xie X et al (2021) Dysregulated hematopoiesis in bone marrow marks severe COVID-19. Cell Discov 7:60. https://doi.org/10.1038/s41421-021-00296-9
doi: 10.1038/s41421-021-00296-9
pubmed: 34349096
pmcid: 8335717
Lee MS, Hsieh P-H, Chang Y-H et al (2008) Elevated intraosseous pressure in the intertrochanteric region is associated with poorer results in osteonecrosis of the femoral head treated by multiple drilling. J Bone Joint Surg Br 90B:852–857. https://doi.org/10.1302/0301-620X.90B7.20125
doi: 10.1302/0301-620X.90B7.20125
Mont MA, Carbone JJ, Fairbank AC (1996) Core decompression versus nonoperative management for osteonecrosis of the hip. Clin Orthop 324:169–178. https://doi.org/10.1097/00003086-199603000-00020
doi: 10.1097/00003086-199603000-00020
Miyanishi K, Yamamoto T, Irisa T et al (2002) Bone marrow fat cell enlargement and a rise in intraosseous pressure in steroid-treated rabbits with osteonecrosis. Bone 30:185–190. https://doi.org/10.1016/S8756-3282(01)00663-9
doi: 10.1016/S8756-3282(01)00663-9
pubmed: 11792583
Liu L-H, Zhang Q-Y, Sun W et al (2017) Corticosteroid-induced osteonecrosis of the femoral head: detection, diagnosis, and treatment in earlier stages. Chin Med J (Engl) 130:2601–2607. https://doi.org/10.4103/0366-6999.217094
doi: 10.4103/0366-6999.217094
pubmed: 29067959
Chan MHM, Chan PKS, Griffith JF et al (2006) Steroid-induced osteonecrosis in severe acute respiratory syndrome: a retrospective analysis of biochemical markers of bone metabolism and corticosteroid therapy. Pathology (Phila) 38:229–235. https://doi.org/10.1080/00313020600696231
doi: 10.1080/00313020600696231
Gedam P, Vallamshetla VRP (2021) A case report on steroid-induced Avascular Necrosis treated with autologous adult live-cultured osteoblasts (AALCO) in COVID-19 patients. SSRN Electron J. https://doi.org/10.2139/ssrn.3929357
doi: 10.2139/ssrn.3929357
Thannheimer A, von Rüden C (2022) Aseptische osteonekrose des medialen femurkondylus bei einem patienten mit akuter SARS-CoV-2 Infektion. Unfallchirurgie 125:664–666. https://doi.org/10.1007/s00113-021-01082-8
doi: 10.1007/s00113-021-01082-8
pubmed: 34586423
Malinowski K, Skowronek P, Hirschmann M et al (2022) Transient spontaneous osteonecrosis of the knee (SONK) shortly after SARS-CoV-2 infection: a report of 2 cases. Adv Clin Exp Med 31:1035–1041. https://doi.org/10.17219/acem/153004r
doi: 10.17219/acem/153004r
pubmed: 36135812
Angulo-Ardoy M, Ureña-Aguilera Á (2021) Knee osteonecrosis after COVID-19. Fam Pract 38:i45–i47. https://doi.org/10.1093/fampra/cmab063
doi: 10.1093/fampra/cmab063
pubmed: 34448481
Agarwala SR, Vijayvargiya M, Sawant T (2022) Secondary osteonecrosis of the knee as a part of long COVID-19 syndrome: a case series. BMJ Case Rep 15:e248583. https://doi.org/10.1136/bcr-2021-248583
doi: 10.1136/bcr-2021-248583
pubmed: 35351759
pmcid: 10577750
Agarwala S, Vijayvargiya M, Sawant T, Kulkarni S (2022) Bisphosphonates for Post-COVID osteonecrosis of the femoral head: medical management of a surgical condition. JBJS Open Access. https://doi.org/10.2106/JBJS.OA.22.00060
doi: 10.2106/JBJS.OA.22.00060
pubmed: 36420354
pmcid: 9678628
Kamani S, Lakhwani MG, Phansopkar P (2022) Undiagnosed bilateral avascular necrosis of the femur in a young male caused by COVID-19 steroid injections. Cureus. https://doi.org/10.7759/cureus.29982
doi: 10.7759/cureus.29982
pubmed: 36381929
pmcid: 9636844
Kingma TJ, Hoch V, Johnson C, Chaudhry B (2022) Avascular Necrosis of the Hip: a Post COVID-19 Sequela. Cureus. https://doi.org/10.7759/cureus.29976
doi: 10.7759/cureus.29976
pubmed: 36582569
pmcid: 9794908
Annam P, Manda A, Myneni UK et al (2022) Corticosteroids induced avascular necrosis of hip, a “long COVID-19” complication: Case report. Ann Med Surg. https://doi.org/10.1016/j.amsu.2022.104753
doi: 10.1016/j.amsu.2022.104753
Maharjan G, Yadav S, Yadav MK et al (2022) Steroid-induced avascular necrosis: A case report on a patient treated with steroid therapy for COVID-19. Ann Med Surg. https://doi.org/10.1016/j.amsu.2022.104226
doi: 10.1016/j.amsu.2022.104226
Agarwala SR, Vijayvargiya M, Pandey P (2021) Avascular necrosis as a part of ‘long COVID-19.’ BMJ Case Rep 14:e242101. https://doi.org/10.1136/bcr-2021-242101
doi: 10.1136/bcr-2021-242101
pubmed: 34215639
pmcid: 8256728
Dhanasekararaja P, Soundarrajan D, Kumar KS et al (2022) Aggressive presentation and rapid progression of osteonecrosis of the femoral head after COVID-19. Indian J Orthop 56:1259–1267. https://doi.org/10.1007/s43465-022-00635-2
doi: 10.1007/s43465-022-00635-2
pubmed: 35495964
pmcid: 9037053
Thankappan A, Nasimudeen N, Thomas A et al (2022) An unusual case of metaphyseal osteonecrosis of humerus in a post covid patient: a case report. Pan Afr Med J. https://doi.org/10.11604/pamj.2022.42.244.34337
doi: 10.11604/pamj.2022.42.244.34337
pubmed: 36303824
pmcid: 9587748
Sulewski A, Sieroń D, Szyluk K et al (2021) Avascular Necrosis bone complication after active COVID-19 infection: preliminary results. Medicina (Mex) 57:1311. https://doi.org/10.3390/medicina57121311
doi: 10.3390/medicina57121311